Relationship of elongated styloid process in digital panoramic radiography with carotid intima thickness and carotid atheroma in Doppler ultrasonography in osteoporotic females.

STATEMENT OF THE PROBLEM
Cardiovascular disease and osteoporosis are major health dilemmas. Osteoporotic patients frequently display vascular calcification that consequently increases the cardiovascular morbidity and mortality.


PURPOSE
This study aimed to investigate the relation of osteoporosis, vascular calcification (atheroma, intima-media thickness (IMT)) and elongated styloid process (ESP) in a sample of osteoporotic and normal female individuals.


MATERIALS AND METHOD
This study recruited 78 women who were assessed for bone mass density (BMD). Sample included individuals with normal BMD (n=13, 17 %), osteopenia (n=36, 46 %), and osteoporosis (n=29, 37%). The presence of atheroma and IMT was examined using color Doppler ultrasonography (CD-US). In addition, digital panoramic radiographs (PRs) were obtained to assess ESP.


RESULTS
In this study, 55 subjects (70%) with low BMD exhibited at least one side ESP. Femoral BMD decreased significantly in subjects with ESP (p= 0.03). Bilateral ESP was correlated with the presence of atheroma (p= 0.029). The CIMT was greater in patients with ESP, although the relation was not significant.


CONCLUSION
The obtained data suggest referring the aged individuals with ESP for BMD assessment and individuals with low bone mass and ESP for more cardiovascular risk assessment.


Introduction
Osteoporosis is a progressive skeletal disease in which the amount of bone is reduced and the trabecular architecture is modified. It is more prevalent in postmenopausal women; however, both men and women with underlying conditions would experience the bone loss. [1] The first study about the association between osteoporosis and oral bone was conducted in 1972. [2] The manifestations of osteoporosis in dentomaxillofacial bone structures include loss of periodontal attachment, [3] loss of teeth, bone loss in the jaws, reduction in the height of alveolar bone, [4] erosion of the inferior mandibular cortex. [5] To the best of authors' knowledge, there is only one English study regarding the relationship of osteoporosis and elongation of styloid process and presence of atheroma. [6] Styloid process is a long cartilaginous bony projection placed on the temporal bone, just anterior to the stylomastoid foramen. [7] The average normal length of the styloid process varies from 20 to 25 mm. The styloid process is assumed to be elongated if it is longer than 30mm. [8][9] Cardiovascular disease and osteoporosis are considered as major health problems. Epidemiological studies suggest that the underlying pathophysiologic mechanisms are similar in osteoporosis and cardiovascular disease. [10][11][12][13][14] Increasing in the intima-media thickness (IMT) is known to be related to the increased risk of myocardial infarction and ischemic stroke. [15] Also, it is related inversely to the lumbar spine BMD in postmenopausal women. [16] Furthermore, low bone mass is associated with echogenic carotid plaques assessed by Doppler ultrasonography. [17] Regarding the limited studies that support the association between the osteoporosis and elongation (calcification) of the stylohyoid complex and vascular calcification, [6,18] the current study aimed to scrutinize the presence of ESP in digital panoramic radiographs (PRs) [19] and carotid atheroma as well as IMT in CD-US in osteoporotic patients versus normal group. This study employs a gold standard method, [20] color Doppler ultrasonography (CD-US), to evaluate the vascular calcification. It will also investigate the associations between the ESP and vascular calcifications and osteoporosis.

Materials and Method
In this study, 95 subjects were recruited from the referees to the bone densitometry center (Namazi Hospital, Iran) during April to November 2011. This study was in compliance with the Helsinki Declaration; all participants were completely informed about the details of the study and relevant consent forms were signed after proper information.
The exclusion criteria were: 1) having unknown precise medical history; 2) tobacco or alcohol use; 3) patients with metabolic bone diseases (such as hyperparathyroidism, hypoparathyroidism); 4) use of med-ications that affect bone metabolism (such as corticosteroid); 5) having any disease that affects cardiovascular system (such as diabetes, hypertension, hyperlipidemia and so on).

BMD Assessment
BMD at the lumbar vertebrae (L2-L4), hip and neck of the femur was determined using dual energy x-ray absorptiometry (DXA, LUNAR DPX IQ). The BMD results of post-menopausal patients were expressed as standard deviations from the bone mass scores of the young female patients participated in the same study (Tscore).
According to WHO criteria, they were classified as: Normal; with BMD ≥−1 standard deviations (SD) from young adult mean, Osteopenia; with BMD ranging from -1 to -2.5 SD below the young adult mean, and Osteoporosis; with BMD ≤-2.5 SD from the young adult mean.

Panoramic radiographs (PRs)
The digital panoramic radiographs were taken by em-  To reduce the intra-observer bias, measurements were repeated after 3 weeks for a total of 20 panoramic radiographs, randomly allocated. Deviations of the mean length of SP between the first and second measurements were 1.5%.

Color Doppler Ultrasonography (CD-US)
Finally, the patients were referred to radiology depart- The presence of atheroma was then assessed by color Doppler.

Statistical Analysis
Predictive Analysis Software (PASW, (SPSS version 15)) was employed to analyze the results. The subjects were divided into 2 groups based on the BMD of the femoral, spinal and hip. The subjects with normal BMD were assigned group 0 and subjects with low BMD (osteopenia, osteoporosis) were allocated group 1.
The subjects were also divided into 2 groups based on the measurement of styloid process; normal length (0= <30mm) and elongated styloid process (1= ≥30mm). Furthermore, they were classified into 2 groups according to the presence of atheroma; 0=no atheroma, 1= presence of atheroma. Pearson's correlation coefficient and t-test were employed to evaluate the association between the hip, femoral and spinal BMD, carotid intima-media thickness, atheroma and elongated styloid process.

Results
The study participants were 78 females and 2 males  Table 1.

Relationship between BMD and ESP
In the correlation analysis, association was found between femoral BMD and the elongation of right styloid process (r=-0.243; p= 0.030). However, in cases where the osteoporosis was detected on all three analyzed sites

Relationship between BMD and IMT
The relationship between IMT and spine, hip and femur BMD was not statistically significant (p= 0.652). But the IMT was higher in subjects with low bone mass than normal BMD subjects.

Relationship of ESP with Atheroma, IMT
A total of 12 atheroma cases were detected in CD-US, IMT was greater in patients with styloid process longer than 30 mm. However, the correlation between IMT and elongated styloid process was not statistically significant (p> 0.05).

Discussion
This cross-sectional study confirmed that extra-osseous bone formation, [22] namely vascular and stylohyoid calcification is prevalent in osteopenic and osteoporotic adults. Panoramic radiography, as a routine radiological evaluation in dental practices, allows practitioners to analyze components of the stomatognathic system as well as other near structures. It is possible to identify and measure the length of styloid process of the temporal bone by this technique, using the images of the external acoustic meatus and tympanic plate as the reference points. [21] Therefore, ESP can be easily detected on these radiographs.
Mineralization or ossification of the styloid process is a common finding. In analysis of digital panoramic radiographs, Chandramani and Mukesh reported 19.4% incidence of ESP. [23] The prevalence in Iranian population was reported to be 36.4% according to the study by Ghafari et al. [24] Calcified styloid processes were more common in patients between 50 and 69 years.
[25] The rate of ESP in Iranian individuals (>40 years old) was 45.6%. [26] Our study showed that 43 of 49 patients (89%) in the age group between 51 to 65 years had at least one elongated styloid process, which is in accordance with the results of other studies. [25][26][27] The first investigation on the relationship between ESP, vascular calcification and osteoporosis was carried out in 2010. [6] According to the study by Watanabe They suggested that SPE may be a predictor of high BMD and high serum calcium level. [18] Atheroma was reported from 2% to 5% in adult population, with a higher frequency rate in menopause women and in individuals aged 65 years and more. [28] A recent investigation in osteoporotic patients, using digital panoramic radiographs, demonstrated 8% incidence (four patients) of vascular calcification, [6] while an incidence of atheroma in this study was 15% (twelve patients

Conclusion
The panoramic radiological images which can provide imperative information on general health condition of the patient can disclose the ESP (ectopic calcification) and reveal its possible relation with the presence of osteoporosis.
Based on the results yielded by this study, an association was found between ESP and osteoporosis and also between ESP and presence of atheroma. The authors would suggest referring individuals (> 40 years old) with ESP for BMD assessment. They also recommend referring the individuals with low bone mass and ESP for further cardiovascular assessment due to the potential risk of atheroma. Further studies, enrolling larger normal and osteoporotic BMD samples, are recommended.